Zoo Biology 28:6974 (2009)

BRIEF REPORT

First Observations of Nest Attendance Behavior by Wild Maned Wolves, Chrysocyon brachyurus
lio Lima Sa bato,1 Luiz Fernando Bandeira De Melo,1 Marco Aure Elisa M. Vaz Magni,1 Robert John Young,2 and Carlyle Mendes Coelho1
1 2

nica, Belo Horizonte, Minas Gerais, Brazil o Zoo-Bota Fundac -a dio 41, Mestrado em Conservation, Ecology and Animal Behaviour Group, Pre lica de Minas Gerais, Belo Horizonte, Minas cia Universidade Cato Zoologia, Pontif Gerais, Brazil
In many species of canids the males role in reproduction extends to providing extensive or some parental care to his offspring. Maned wolves are a monogamous canid species whose males have been observed providing parental care to their offspring in captivity, but no eld observations exist. We observed a wild pair of maned wolves at their nest site in a period soon after the female had given birth for a total period of 65 days. We made ve observation sessions with an average of 34 days each separated by approximately 2 weeks. Direct visual observations of maned wolves were made each 30 min during the hours of darkness (17:0007:00) using nightvision binoculars and conrmed by VHF radiotelemetry. During observations we recorded the location of the male and the female in relation to the nest (i.e., in the nest, nearby or long way from the nest). The results showed that the female spent more than 60.44% of her time in or near the nest. The male spent 28.90% of his time in or near the nest. There was a positive signicant correlation between the female and the male in terms of the amount of time spent in or near the nest (Po0.01). The maned wolves showed a strong temporal variation in time spent in or near the nest. In conclusion, our data show that wild male maned wolvesprobablyprovide parental care through provision of food to their female and presumed offspring rather than babysitting. Zoo Biol 28:6974, 2009. r 2008 Wiley-Liss, Inc.

Keywords: canids; male behavior; parental care

Grant sponsor: CEMIG.
Correspondence to: Robert John Young, Conservation, Ecology and Animal Behaviour Group, Pre dio lica de Minas Gerais, Av. Dom Jose Gaspar, 500 41, Mestrado em Zoologia, Pontif cia Universidade Cato Corac -a o Eucar stico, 30535-610 Belo Horizonte, Minas Gerais, Brazil. E-mail: robyoung@pucminas.br

Received 9 August 2007; Revised 31 July 2008; Accepted 31 July 2008 DOI 10.1002/zoo.20213 Published online 4 November 2008 in Wiley InterScience (www.interscience.wiley.com).

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INTRODUCTION The maned wolf is a large monogamous species of canid, which inhabits much of South America. Knowledge concerning its behavior in the wild is lackingmost wild studies have concentrated on investigating the species diet [see de Melo et al., 2007]. Therefore, information concerning all aspects of wild behavior of this species is of great importance, especially considering the fact that although not in one of the most endangered categories of the IUCN Red Listnear threatened [Sillero-Zubiri and Hoffmann, 2004]its principal habitat, the Brazilian cerrado, is one of the worlds biodiversity hot spots [Myers et al., 2000], and as such it is under threat. Canids are unusual among the carnivores in that many species are monogamous and parental care is often well developed [Asa and Valdespino, 1998]. In small insectivorous canids such as the hoary fox (Pseudalopex vetulus) or the raccoon dog (Nyctereutes procyonoides), males often spend a considerable amount of their time budget caring for their offspring [Courtenay et al., 2006; Kauhala et al., 1998]. This is thought to be owing to the difculty males have in bringing insect prey items back to their females or offspring. However, in larger species such as the maned wolf, who do not express cooperative hunting, one would predict that males could bring prey items back to their females and offspring. Therefore, we would expect them to spend less time at the nest as there would be little need for them to babysit their offspring while their mate was hunting. Studies in captivity have shown that male maned wolves provide a range of parental care including protecting their offspring and providing food for their offspring and mates [Dietz, 1984; Veado, 1997]. However, as stated in the IUCN Canid Action Plan [2004], the role that the male plays in parental care in the wild is yet to be conrmed. Recently, de Melo et al. [2007] have shown that males associate extensively with their females before, during and after the breeding season; however, in their study the males presence in the nest was not visually conrmed. Owing to the continuing destruction of the maned wolves prime habitatthe Brazilian cerradoa captive breeding program for the species is considered necessary [Sillero-Zubiri and Hoffmann, 2004]. However, one of the main problems with the captive breeding program for this species has been males attacking their offspring, leading some zoos to separate males from their offspring [Maia and Gouveia, 2002]. Although this may increase infant survival, it is contrary to recent wild observations, which show that the male and the female have a pronounced association during the breeding season [de Melo et al., 2007]. Here, we report radiotelemetry and direct behavioral observations made of male and female maned wolf activity at a nest with offspring. The observations include a period from soon after the birth of the offspring until approximately 65 days of age.

MATERIALS AND METHODS The subject of our study was a mated pair of wild maned wolves. This study was conducted in the RPPN Serra do Carac - a Private Natural Heritage Reserve (201050 S, 431290 W) located in Minas Gerais State, south-eastern Brazil. The area of the reserve is 10,187.89 ha, with altitudes ranging from 850 to 2,072 m, and is situated in the southern portion of the Espinhac - o Mountain range. This orographic system is
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represented by a mountainous complex that delimits a zone of contact between the cerrado (Brazilian savannah) and the Atlantic Forest in its southern portion and transition zones of cerrado, Atlantic Forest and caatinga (tropical deciduous forest) in its central and northern edges. In the center of the reserve is a hotel where supplemental feeding (approximately 2 kg of meat per day) of the maned wolves occurred on a nightly basis between 19:00 and 22:00 hr. The reserve and the supplemental feeding have been described in detail by Silva and Talamoni [2004]. Our study was conducted from June 2001 until August 2001 for a period of 65 days. The maned wolves had been previously captured and tted with VHF radio collars (model Simplex manufactured by Televilt, Lindesberg, Sweden; Coelho et al., 2007). Using the radio collars we were able to locate the reproductive nest of this pair of maned wolves. The wolves were using a large hollowed out termite mound in a cerrado area of the reserve as their nest, which during our observations contained only one pup. Unfortunately, this nest site meant that we could not directly observe the behavior in the nest. We observed the maned wolves only during the hours of darkness to avoid excessive disturbance at the nest. The wolves locations were conrmed using their radio collars and when possible were observed using a night-viewing binocular (Nightowl Explorerr El Paso, Texas), which permitted us to identify and conrm the presence of an adult maned wolf in or near the nest. However, we were not able to see the behavior of the wolves in the nest. Therefore, we recorded the following variables every 30 min: the identity and location of each adult (in the nest, near the nest (o100 m) (in visual contact) or a long way from the nest (4100 m) (out of visual contact)). The wolves were observed in ve separate periods of observations from June to August 2001 (see Table 1). The length of the observation period was based on previous observations, which showed that at approximately 70 days of age, pups start to accompany their mothers on hunting trips [see also de Melo, 2007]. For each observation period we calculated the mean amount of time each wolf spent in or near the nest (see Table 1). To examine the effect of time of day we used all of the available data to calculate a mean percentage of time that each wolf was in or near the nest per hour (see Fig. 1). An AndersonDarling test of our data revealed a nonnormal distribution and, therefore, all statistical tests applied were nonparametric. Specically, we used the Spearman rank correlation to investigate relationships between percentage of observations at the nest by the adults and time of day or the presence of the other adult. All data were analyzed in the statistical software Minitab version 12.

TABLE 1. Mean time in percentage (7SEM) spent in or near the nest by adult maned wolves in relation to the ve observation periods Observation period June 1821 July 25 July 1618 July 30August 1 August 1316 Female mean (%) 71.43710.9 45.45720.6 43.91710.7 61.41715.7 80.0075.69 Male mean (%) 30.35716.8 29.09714.0 24.40711.0 31.5877.51 29.09715.2

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100 Percentage of observations 80 60 40 20 0 0 1 2 3 4 5 6 17 18 19 20 21 22 23 Time of day Female Male

Fig. 1. Time spent (in percentage of observations) in or near the nest by adult maned wolves in relation to time of day.

RESULTS We made 264 observations of adult presence or absence at the nest during our study. Our results show that on average, during the night, the female was seen in or near the nest for a mean of 60.44% (77.08) (mean7SEM) of the observation time, whereas the male was observed in or near the nest for a mean of 28.90% (71.22) of the observation time. An adult animal was either in or close to the nest for 64.02% of the observation time. Only on seven occasions (2.66%) did we observe the male in or close to the nest, when the female was far away from the nest. Across the ve sequential observation periods we did not detect any effects of time on the percentage of observations spent in or near the nest by the animals (P40.05 in all cases; see Table 1). Male values for nest attendance were relatively constant, whereas female values varied nonsystematically across the observation periods. In relation to time of day, we saw that the female only reduced her presence at the nest between 19:00 and 22:00 hr: a similar pattern was also observed in the male (see Fig. 1). We correlated, using a Spearman rank correlation, the percentage of time in or near the nest for the male and the female in relation to time of day to try and detect if there was any sharing of responsibility for care (a negative correlation would indicate one adult present when the other was distant from the nest). The correlation showed a positive relationship between the male and the female in relation to time of day and presence at the nest (rs 5 0.758; n 5 14; Po0.01). DISCUSSION Despite the small sample size of this study, meaning that the results are not generalizable to all wild maned wolves, we feel that the observations provide important information about a relatively unknown species. These data conrm that in the wild, male maned wolves do play a role in the rearing of their presumed offspring as has been observed in captive studies [Dietz, 1984, 1985; Veado, 1997]. However, the male did not take on the role of babysitter as has been observed in other canid species [e.g., hoary fox; Courtenay et al., 2006]; that is, the male and the female did not take turns in caring for the young. In fact, what we observed was that the male presence at the nest was highly correlated with the female presence, and that
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on only seven occasions was the male alone at the nest with the offspring. These data suggest that, perhaps, the main role of the male was to provide the female and the offspring with food. However, it should be acknowledged that this correlation of male and female presence was highly inuenced by the fact that both the male and the female rested with the pup for almost 100% of the time during daylight hours (personal observations). The female and male resting with their offspring during daylight hours has been observed in maned wolves in other reserves within Brazil [de Melo et al., 2007]. Interestingly, both the male and the female were most likely to be absent from the nest between 19:00 and 22:00 hr. During this period supplemental feeding was offered to the wolves at the sanctuary. From Figure 1 we can see that after taking advantage of this supplemental feeding (personal observations) the female returned to her nest, probably to nurse her offspring or, when they were older, to regurgitate food for them. The male also showed a small peak in nest visitation at around 22:00 hr (Fig. 1), which may have been related to food regurgitation for the female or the pup. However, the male was most likely to be associated with the nest as dawn approached (see Fig. 1). The supplemental feeding means that the adults needed to spend less time searching for food than would otherwise be necessary. Therefore, in our study the time at the nest may be an over-representation in comparison with individuals not submitted to supplemental feeding. During the course of our study a parallel study on the effect of supplemental feeding on the center of activity and the diet of these maned wolves was being undertaken. This study showed that although the wolves did utilize the supplemental food on a daily basis (approximately 30% of their daily intake), they also hunted vertebrate and invertebrate prey and consumed plants [Silva and Talamoni, 2004]. Furthermore, a study of their ecology and habitat selection showed many parameters, such as home range size, to be in accordance with published values for wild maned wolves [see Coelho et al., 2008]. We may therefore conclude that the behavior of these maned wolves was not atypical of the species. However, our data do not permit us to say whether the male parental care observed was facultative or obligate, and this could of course be affected by supplemental feeding [Lott, 1991]. Therefore, local conditions, in terms of food availability, may affect the type and level of parental care behavior expressed by males. Our data suggested that the male did play an important role in rearing his presumed offspring, but that the partnership between the male and the female was not equal with the female spending much more time in the nest. This probably reects the fact that the male could bring prey items or supplemental food to the nest [see Kauhala et al., 1998]. It may of course be that the male was performing other important roles necessary for the survival of offspring such as territorial marking. In the parallel study of Silva and Talamoni [2004] the maned wolves deposited many feces close to the sanctuary where the supplemental feeding was taking place. Dietz, based on his studies of wild maned wolves in Brazil (1984, 1985), suggests that individuals place feces to mark their territory. However, this theory has not been tested experimentally. One further observation that deserves comment is that the male was rarely alone at the nest with his presumed offspring. This could be owing to the absence of the female (i.e., no need for provisioning of food). Alternatively, it could be that the female, specically, did not leave the pup in the care of the male: studies in captivity have reported males attacking their pups [Maia and Gouveia,
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2002]; however, on no occasion did we observe the male showing any aggressive behavior toward the pup or detect nervousness in the female when the male was approaching the nest. CONCLUSIONS 1. Wild male maned wolves participate in the care of their offspring. 2. It is rare for a male to be left on his own with his offspring.

ACKNOWLEDGMENTS lio and Sebastia We thank Padres Ce - a Private o, and Consuelo from Carac Nature Reserve for giving us permission to conduct our study in their reserve. The research in this paper was generously funded by CEMIG (Energy Company of Minas Gerais). The research in this paper was conducted in compliance with all relevant state and federal laws in Brazil. We also thank IBAMA for the license to conduct this research. REFERENCES
Asa CS, Valdespino C. 1998. Canid reproductive biology: an integration of proximate mechanisms and ultimate causes. Am Zool 38:251259. bato MAL, NoCoelho CM, de Melo LFB, Sa gueira DR, Young RJ. 2007. A note on the use of GPS collars to monitor wild maned wolves Chrysocyon brachyurus (Illiger 1815) (Mammalia, Canidae). Appl Anim Behav Sci 105:259264. bato MAL, Magni Coelho CM, de Melo LFB, Sa EMV, Hirsch A, Young RJ. 2008. Habitat use by wild maned wolves (Chrysocyon brachyurus) in a transition zone environment. J Mammal 89:97104. Courtenay O, Macdonald DW, Gillingham S, Almeida G, Dias R. 2006. First observations on South Americas largely insectivorous canid: the hoary fox (Pseudalopex vetulus). J Zool 268:4554. bato MAL, Magni EMV, Young de Melo LFB, Sa RJ, Coelho CM. 2007. The secret lives of maned wolves Chrysocyon brachyurus Illiger 1815: as revealed by GPS tracking collars. J Zool 271:2736. Dietz JM. 1984. Ecology and social organization of the maned wolf (Chrysocyon brachyurus). Smithsonian Contrib Zool 392:151. Dietz JM. 1985. Chrysocyon brachyurus. Mamm Species 234:14. IUCN Canid Specialist Group. 2004. Canids: foxes, wolves, jackals and dogs status survey and conservation action plan. Cambridge: IUCN Publications Services Unit. Kauhala K, Helle E, Pietila H. 1998. Time allocation of male and female raccoon dogs to pup rearing at the den. Acta Theriol 43: 301310. Lott DF. 1991. Intraspecic variation in the social systems of wild vertebrates. Cambridge: Cambridge University Press. Maia OB, Gouveia AGM. 2002. Birth and mortality of maned wolves Chrysocyon brachyurus (Illiger, 1811) in captivity. Braz J Biol 62:2532. Myers N, Mittermeier RA, Mittermeier CG, Da Fonseca GAB, Kent J. 2000. Biodiversity hotspots for conservation priorities. Nature 403: 853858. Sillero-Zubiri C, Hoffmann M. 2004. Chrysocyon brachyurus. IUCN 2004. 2004 IUCN Red List of Threatened Species /www.iucnredlist.orgS. Downloaded on 3 May 2007. Silva JA, Talamoni SA. 2004. Core area and centre of activity of maned wolves, Chrysocyon brachyurus (Illiger) (Mammalia, Canidae), submitted to supplemental feeding. Rev Bras Zool 21:391395. Veado BV. 1997. Parental behaviour in maned wolf Chrysocyon brachyurus at Belo Horizonte Zoo. Int Zoo Year 35: 279286.

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